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Hamilton’s theory of inclusive fitness showed how natural selection could lead to behaviors that decrease the relative fitness of the actor and also either benefit (altruism) or harm (spite) other individuals. However, several fundamental issues in the evolution of altruism and spite have remained contentious. Here, we show how recent work has resolved three key debates, helping clarify how Hamilton’s theoretical overview links to real-world examples, in organisms ranging from bacteria to humans: Is the evolution of extreme altruism, represented by the sterile workers of social insects, driven by genetics or ecology? Does spite really exist in nature? And, can altruism be favored between individuals who are not close kin but share a “greenbeard” gene for altruism?
Explaining altruistic cooperation is one of the greatest challenges for evolutionary biology1,2,3. One solution to this problem is if costly cooperative behaviours are directed towards relatives4,5. This idea of kin selection has been hugely influential and applied widely from microorganisms to vertebrates2,3,4,5,6,7,8,9,10. However, a problem arises if there is local competition for resources, because this leads to competition between relatives, reducing selection for cooperation3,11,12,13,14. Here we use an experimental evolution approach to test the effect of the scale of competition, and how it interacts with relatedness. The cooperative trait that we examine is the production of siderophores, iron-scavenging agents, in the pathogenic bacterium Pseudomonas aeruginosa15,16,17. As expected, our results show that higher levels of cooperative siderophore production evolve in the higher relatedness treatments. However, our results also show that more local competition selects for lower levels of siderophore production and that there is a significant interaction between relatedness and the scale of competition, with relatedness having less effect when the scale of competition is more local. More generally, the scale of competition is likely to be of particular importance for the evolution of cooperation in microorganisms, and also the virulence of pathogenic microorganisms, because cooperative traits such as siderophore production have an important role in determining virulence6,9,17,18,19.
Hamilton's inclusive fitness theory represents one of the most important developments in evolutionary biology. In particular, the idea that individuals benefit from the reproduction of relatives (kin selection) has been extraordinarily successful in explaining a wide range of phenomena, especially cases of supposed altruism. However, recent work has emphasized how the importance of kin selection can be overestimated ? an estimate of high relatedness between interacting individuals is not in itself sufficient evidence that kin selection is responsible for promoting altruism. In particular, supposedly altruistic traits can have direct fitness benefits, and competition between relatives can reduce the importance of indirect fitness benefits.
The occurrence of cooperation poses a problem for the biological and social sciences. However, many aspects of the biological and social science literatures on this subject have developed relatively independently, with a lack of interaction. This has led to a number of misunderstandings with regard to how natural selection operates and the conditions under which cooperation can be favoured. Our aim here is to provide an accessible overview of social evolution theory and the evolutionary work on cooperation, emphasising common misconceptions.
AbstractOur understanding of the social lives of microbes has been revolutionized over the past 20 years. It used to be assumed that bacteria and other microorganisms lived relatively independent unicellular lives, without the cooperative behaviors that have provoked so much interest in mammals, birds, and insects. However, a rapidly expanding body of research has completely overturned this idea, showing that microbes indulge in a variety of social behaviors involving complex systems of cooperation, communication, and synchronization. Work in this area has already provided some elegant experimental tests of social evolutionary theory, demonstrating the importance of factors such as relatedness, kin discrimination, competition between relatives, and enforcement of cooperation. Our aim here is to review these social behaviors, emphasizing the unique opportunities they offer for testing existing evolutionary theory as well as highlighting the novel theoretical problems that they pose.